Chronotype variation drives night-time
rspb.royalsocietypublishing.org
Research
Cite this article: Samson DR, Crittenden AN,
Mabulla IA, Mabulla AZP, Nunn CL. 2017
Chronotype variation drives night-time
sentinel-like behaviour in hunter – gatherers.
Proc. R. Soc. B 284: 20170967.
http://dx.doi.org/10.1098/rspb.2017.0967
Received: 5 May 2017
Accepted: 7 June 2017
Subject Category:
Behaviour
Subject Areas:
behaviour, ecology, evolution
Keywords:
sleep, sentinel, chronotype, actigraphy,
hunter – gatherer, evolutionary mismatch
Author for correspondence:
David R. Samson
e-mail: david.samson@gmail.com
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.3811684.
sentinel-like behaviour in hunter –
gatherers
David R. Samson1,6, Alyssa N. Crittenden2, Ibrahim A. Mabulla3,
Audax Z. P. Mabulla4 and Charles L. Nunn5,6
1
Department of Anthropology, University of Toronto, Mississauga, Mississauga, Ontario, Canada M5S 2S2
2
Department of Anthropology, University of Nevada, Las Vegas, Las Vegas, NV, USA
3
Institute of Resource Assessment, and 4Department of Archaeology and Heritage, University of Dar es Salaam,
Dar es Salaam, Tanzania
5
Duke Global Health Institute, and 6Department of Evolutionary Anthropology, Duke University, Durham,
NC 27708, USA
DRS, 0000-0003-3318-7652; ANC, 0000-0001-9196-737X; CLN, 0000-0001-9330-2873
Sleep is essential for survival, yet it also represents a time of extreme
vulnerability to predation, hostile conspecifics and environmental dangers.
To reduce the risks of sleeping, the sentinel hypothesis proposes that group-
living animals share the task of vigilance during sleep, with some individuals
sleeping while others are awake. To investigate sentinel-like behaviour in
sleeping humans, we investigated activity patterns at night among Hadza
hunter–gatherers of Tanzania. Using actigraphy, we discovered that all subjects
were simultaneously scored as asleep for only 18 min in total over 20 days of
observation, with a median of eight individuals awake throughout the night-
time period; thus, one or more individuals was awake (or in light stages of
sleep) during 99.8% of sampled epochs between when the first person went
to sleep and the last person awoke. We show that this asynchrony in activity
levels is produced by chronotype variation, and that chronotype covaries
with age. Thus, asynchronous periods of wakefulness provide an opportunity
for vigilance when sleeping in groups. We propose that throughout human
evolution, sleeping groups composed of mixed age classes provided a form of
vigilance. Chronotype variation and human sleep architecture (including noc-
turnal awakenings) in modern populations may therefore represent a legacy of
natural selection acting in the past to reduce the dangers of sleep.
1. Introduction
In 1966, Frederick Snyder [1] proposed the sentinel hypothesis (p. 130): ‘Man and
other animals have learned that under conditions of danger it is safe to sleep
only if sentinels are employed to remain vigilant. . ..’ He further proposed that
periodic awakenings associated with shifts between NREM and REM sleep
served the purpose of providing individuals with scan samples of their environ-
ments. In a group situation, vigilance behaviour could be achieved through
behavioural mechanisms to ensure that some individuals serve as sentinels
while others sleep. Sentinel-like behaviour could also be achieved through vari-
ation in sleep timing, periodic awakenings, and periods of time spent in lighter
stages of sleep, from which arousals would be more likely in the context of exter-
nal threatening stimuli. For example, if some individuals in a group go to sleep
early and wake up earlier than other individuals, this would facilitate greater
levels of wakefulness at the beginning and end of the sleep period.
Although research on human vigilance behaviour remains largely unexplored
[2], work on circadian rhythmicity and sleep homeostasis has investigated
individual differences in sleep–wake regulation, revealing high variance in
phase timing (i.e. the preference for a given sleep start and end time) consistent
with humans having different chronotypes (defined as the individual propensity
& 2017 The Author(s) Published by the Royal Society. All rights reserved.
for sleep and activity at particular times during a 24 h period) [3].
Individuals in the tails of the distribution are colloquially known
as morning ‘larks’ and night ‘owls,’ reflecting that they either go
to sleep early and wake early, or go to sleep late and wake late.
Chronotype variation is found across animals; examples include
the existence of stable, species-typical chronotypes in birds [4,5]
and rodents [6], and the chronotype of the diurnal degus
(Octodon degus) is described as similar to humans [7].
In Western populations, the chronotype distribution is nor-
mally distributed, sex-specific (with males biased towards
being late chronotype) and characterized by systematic
changes to chronotype across the lifespan (with older individ-
uals tending to be more early chronotype) [8]. Chronotype
variation is independent of total sleep duration [8] and has
been shown to correlate with physiological measures, such as
early low core body temperature [9,10], greater melatonin
secretion [11], higher cortisol levels [12] and lower testosterone
[13] in early morning types. The genetic basis of chronotype
variation has been investigated, with twin studies showing
that chronotype is moderately to highly heritable (40–72%)
[14], and circadian rhythmicity has been linked with PERIOD
genes [15] and the circadian clock gene CRY1 [16].
Individual differences in sleep behaviour have been
interpreted as variation that is linked to circadian phase misa-
lignment, resulting in health problems and often identified as a
sleep disorder when the misalignment is extreme [17]. Recent
investigations reframe this disease-focused perspective in the
context of evolutionary mismatch, where changes in environments
and lifestyles today differ from those in our ancestral past in ways
that create evolutionarily novel health challenges [18]. Thus,
investigating sleep phasing in nonindustrial humans is not
only important to basic science, but may also provide advances
in understanding some human sleep disorders.
To investigate group-level sleep patterns in a system rel-
evant to our human evolutionary past, we studied Hadza
hunter–gatherers. The Hadza live in a savannah-woodland
environment in Northern Tanzania, and their foraging lifestyle
has been thoroughly documented [19]. The activity patterns of
their society are not regulated from a structured ‘top–down’
system that assumes work during specific times during the
day. Additionally, this population lacks environmental barriers;
such barriers are standard in post-industrial society, includ-
ing environmentally controlled buildings with insulation that
blunts noise and other critical zeitgebers (e.g. artificial light)
that have been previously demonstrated to influence circadian
timing of activity or inactivity. With very little if any aid from
industrially produced equipment or tools, they hunt and
gather on foot using bows, digging sticks, and axes. Sexual
division of foraging effort is pronounced, with men hunting
for game and spending considerable effort gathering honey,
while women gather plant products [20]. While no living
population is a perfect model of ancestral lifestyles, Hadza sub-
sistence strategy and ecology are thought to offer important
similarities to our Pleistocene ancestors [19].
We investigate the possibility that, under the sentinel
hypothesis, phenotypic variation in sleep timing may have
been adaptive in ancestral human environments, where
night-time wakefulness could have increased group-level
vigilance and survivability as a way to counter outside
threats from predators, environmental hazards and hostile
conspecifics. We predict that only rarely will all individuals
in a group be identified as asleep during night-time periods
based on actigraphy, which scores sleep based on movement
patterns that correspond with wakefulness or light sleep. 2
Alternatively, if all individuals in the study tend to be asleep
rspb.royalsocietypublishing.org
simultaneously for long intervals of time, the sentinel hypo-
thesis would be rejected. To test this general prediction, we
developed a simulation model to produce a null distribution
of wakefulness overlap that is tailored to our sampling
regime and data. Empirical observations of more extreme vari-
ation in wakefulness overlap would support the sentinel
hypothesis. We further used this model to investigate the fac-
tors that influence sleep synchrony, focusing on variation in
chronotype and group size. Finally, to assess whether demo-
graphic and other factors maintain chronotype variation, we
Proc. R. Soc. B 284: 20170967
investigated how age, sex, number of co-sleeping children,
weather and nursing status predict chronotype.
2. Methods
(a) Subjects
The Hadza lie near the median value for most ecological and
life-history traits among equatorial hunter–gatherers [19]. For
example, they live in an East African environment with an effective
temperature of 178C, which is close to the median for warm-
climate hunter– gatherers (16.38C). Average annual temperature
varies considerably between day and night (mean min ¼ 148C,
mean max ¼ 358C), but little across the year (mean  288C). Habi-
tat is primarily savannah–woodland, with the inclusion of rocky
hills, brush and marshland [19]. Their environment is highly seaso-
nal, with the dry season occurring between June and November
and the wet season occurring from December to May, with short
rains followed by long rains.
The annual Hadza diet consists of approximately 43% hunted
foods (game animals, birds and honey) and 57% gathered foods,
including fruits, legumes, tubers, and nuts and seeds [21], similar
to the median value for the diets of other African hunter–gatherers
[19]. The median local group home range for the Hadza is 122 km2,
although range sizes are declining due to adjacent population
pressure and globalization [22,23]. Importantly, the median local
group size is approximately 30 for the Hadza (mean group size
for warm-climate hunter–gatherers is 26), and groups are charac-
terized by central-place provisioning, with individuals returning
to a central place to distribute food [20]. The Hadza exhibit high
levels of sexual division of labour, with males acting as primary
hunters and females as primary gatherers.
Hadza volunteers were recruited from a bush camp located
near Lake Eyasi in northern Tanzania (latitude: 03–048S and longi-
tude 34–368 E). Volunteers participated in the study between June
21 and February 11, 2016. Day length at this time of year ranged
between 12.23 and 12.28 h, sunrise occurred between 06.43 and
06.46, and sunset occurred between 18.59 and 19.00 (http://aa.
usno.navy.mil/data). Lunar phase ranged from full moon to com-
plete cover of lunar light. Participants were healthy adults over 18
years of age who engaged in daily foraging. In addition to age,
exclusion criteria included self-reported insomnia or physical dis-
ability due to injury or infirmed status that prevented an
individual from engaging in active foraging. Based on injury
and infirmed status, three individuals were excluded from analy-
sis; no one was excluded due to insomnia, as no potential subjects
reported sleep difficulties. In total, 33 subjects completed the
study, with up to 22 subjects wearing actigraphs during any
given day. The sample was composed of 21 females (mean age:
34.9 + 14.3 years) and 12 males (mean age: 35.6 + 14.7 years).
All research was approved by the Tanzanian Commission
for Science and Technology (COSTECH) and the Tanzanian
National Institute for Medical Research (NIMR). All eligible
subjects gave their verbal informed consent, as outlined by
the Institutional Review Board for human subjects research at the
University of Nevada, Las Vegas and Duke University. The sleep
survey was based on a previously validated-cross cultural survey
[24] and translated into Swahili (see electronic supplemental
material for the English version of the administered survey).
(b) Protocol
Participants were verbally administered a sleep survey in Swahili,
their second language, at the beginning of the study period
(20 January–11 February 2016) to screen for healthy sleep and
ascertain general information on subjective sleep quality and
threat perception (see electronic supplemental material). During
the initial survey, participants were asked to rank perceived
threats from greatest to least from among a list of five potential cat-
egories: (i) animals, (ii) disease, (iii) lack of food, (iv) people and
(v) weather. When asked to rank perceived threats, subjects
ranked ‘lack of food’ as the most urgent primary threat (48.6%),
‘other people’ (29.7%) as their second most urgent primary threat,
with a tie between ‘animals’ (10.8%) and ‘disease’ (10.8%) for pri-
mary threats; ‘weather’ was perceived as the least dangerous, with
75.7% of respondents putting it in the least threatening category.
Although polysomnography (PSG) is currently considered
the gold standard for quantifying sleep, it remains cumbersome,
expensive and difficult to apply with ambulatory participants in
a primitive field setting. Actigraphy, on the other hand, is a valu-
able approach to investigate sleep outside of clinical or
laboratory settings. The noninvasive, wrist-worn device has
been increasingly adopted to investigate sleep not only in var-
ious populations living in post-industrialized Western societies
[25], and also in developing countries [26,27] and non-industrial-
ized, small-scale societies [28,29].
We used the Motionwatch 8 actigraph (CamNtech). The
MotionWatch 8 sensor logs motion data over a user-defined inter-
val, or epoch, using a built-in tri-axial accelerometer. The sensor
samples data at 50 Hz and accumulates data over the epoch, ulti-
mately assigning it an integer value on a ratio scale (‘counts’).
We collected data on the minute, as continuous 1-min sampling
is the most commonly used actigraphic method for measuring
sleep– wake activity patterns in both human and non-human pri-
mates [30]. Subjects were asked to press the actigraphy event
marker preceding any sleep event throughout the study, including
sleep after night-time wake bouts and before initiating daytime
naps. Actigraph data were scored using the CamNtech Motion-
Ware 1.1.15 program. The software has a sleep detection
algorithm that generates sleep quotas based on actigraphic
counts. The algorithmic high-sensitivity settings are the most com-
monly used in actigraphy sleep studies due to demonstrated
reliability for determining sleep versus wakefulness [25]; therefore,
we used the high-sensitivity setting in this study. By collecting
data on multiple individuals per night, we can control for
environmental variables that might affect sleep.
Although the algorithms score an individual as asleep or
awake in each epoch, we note that many cases of scored wakeful-
ness may actually represent light stages of sleep. We are
assuming here that stimuli occurring during light sleep are
more likely to lead to an arousal, and thus relevant to investi-
gating the sentinel hypothesis, even though we do not have
direct data on wakefulness (which would require EEG or obser-
vation, neither of which are possible in this field setting). The
reasonableness of this assumption is based on studies showing
that subjects awaken easily from light sleep (stages N1 & N2
characterized by the lowest arousal threshold) and tonic REM
[31]. In addition, we note that the algorithms may also score an
awake but still person as sleeping. In this case, however, we
would be underestimating the degree of synchronous wakeful-
ness, making it harder to test the sentinel hypothesis and thus
acting as a conservative bias.
(c) Statistical analyses 3
We used R v. 3.3.0 [32] to conduct statistical analyses. For each
rspb.royalsocietypublishing.org
24 h period throughout the study (n ¼ 20 days), we performed
an epoch-by-epoch analysis, from the phase at which the first
subject fell asleep to the phase at which the last subject awoke.
Sleep epochs were determined by the CamNtech MotionWare
software after the sleep onset and sleep offset periods were desig-
nated manually by an experienced scorer (D.R.S.), guided by the
event markers used by study participants. We generated descrip-
tive statistics reporting the mean wake-ratio ( proportion of
subjects that are awake at any given night-time epoch) and
mean of the median of subjects awake at any given night-time
epoch. We also generated the effective group sleep time, which is
Proc. R. Soc. B 284: 20170967
the sum duration from the first person scored as asleep in the
evening to the last person scored as awake in the morning. More-
over, we calculated and averaged circadian phase measure (CPM)
[3], which is the midpoint of clock time between sleep onset
and awakening.
Functional linear modelling (FLM) was used to characterize
and illustrate 24 h sleep–wake patterns [33]. The FLM approach,
specifically designed for actigraphy time-series data analysis,
measures raw activity counts within and between samples, and
can overcome problems when summary statistics mask differences
across groups. FLM was used to compare activity patterns to assess
the timing of sleep–wake activity on the individual level to ident-
ify periods during the 24 h cycle when all individuals (with Fourier
smoothed averages) were asleep at the same time.
To characterize the most and least active time periods
between sexes, we used Nonparametric Circadian Rhythm
Analysis (NPCRA) [34]. NPCRA does not assume that the data
fit any pre-defined distribution, therefore making it the preferred
method to analyse several consecutive 24 h periods of activity –
rest data (which do not typically fit well with traditional Cosinor
waveform analysis) [34].
We developed a simulation model for comparison to the
empirical data, and to further investigate the underlying mechan-
isms, including the effects of variation in chronotype and group
size on group-level night-time wakefulness patterns. The model
was parameterized to match exactly the data collection, including
variation in the number of subjects sampled per day, and also
using inferences from actigraphy data of transitions from sleep
to wakefulness (or light sleep). The model is based on a discrete
time Markov chain, in which time units correspond to 1-min
epochs in the actigraphy data and the probability of a sleep –
wake state in time t depends on the state in time t 2 1, with tran-
sition probabilities estimated from the collected data. We first
ran this model with all individuals having identical transition
probabilities, sleep onset time and wake time (i.e. no variation in
chronotypes), based on empirical data for one randomly selected
individual on a random day. We ran this model 1000 times, ran-
domly sampling an individual from the empirical dataset for
each 20-day simulation. To introduce variation in chronotypes,
we then repeated the procedure, but using a different individual
to parameterize sleep for each individual simulated per day. We
also used the model to assess how changes in group size affect
sleep synchrony, with and without variation in chronotypes.
These more general simulations were run assuming a constant
number of individuals sampled across nights, for 20 nights.
To investigate the factors that covary with circadian phase
based on CPM, we ran a linear mixed effects model across
390 nights of data. The fixed effects were age, sex, number of
co-sleeping children in the bed, nursing status and study day (con-
trolling for environmental variability). We included ‘subject’ as a
random effect to control for repeated measures. The model was
run using the lme4 package [35] in R, with estimates obtained
using log-likelihood optimization. Using multi-model inference
based on AIC [36], we averaged models with DAIC , 10 using
the MuMIn package [37]. Statistical inferences were made using
standardized coefficient estimates with shrinkage and 95%
confidence intervals.
3. Results
(a) Sleep sites and threat perception
The camp consisted of two subgroups of grass-huts (total
n ¼ 22). The distance between the two groups was 127 m,
measured to the centre of each. The average distance
between huts was 12.7 m, as measured to the closest adja-
cent hut. The average hut size was 1.89 m (s.d. ¼ 0.42) tall,
2.71 m (s.d. ¼ 0.38) in diameter at the base, and with wall
thickness of 0.22 m (s.d. ¼ 0.04). In each hut, on average 3.4
(s.d. ¼ 1.97) individuals slept, including both children and
adults. The average noise level in each cluster was 46.95
(dB), and previous research found that an individual can
raise his or her voice to be heard across clusters [38].
(b) Measuring forager sleep – wake patterns
We found high levels of scored wakefulness at night by the
Hadza. The summary of statistics generated from the night-
time epoch-by-epoch results are presented in the electronic
supplementary material, table S1. The mean (s.d.) wake-ratio
(i.e. the proportion of all participants that were awake at any
given epoch during the night-time period) was 0.394 + 0.08.
In other words, on average 60.6% of the group were scored
as asleep while 39.4% were scored as awake, indicating inferred
wakefulness. On a per-night basis, the median number of indi-
viduals (max n ¼ 22 subjects per night) scored as awake ranged
from 5 to 12, with an overall median of eight individuals awake
at any given time (see electronic material for more detail on
sampling characteristics and a supplemental figure of the
number of individuals awake throughout the sleep period for
each study night). All individuals were simultaneously
scored as asleep for a total of only 18 one-minute epochs over
20 nights (13 408 total epochs, and thus simultaneously
asleep in only 0.002% of analysed epochs). It is important to
note that we were unable to sample every individual in the
camp, and actigraphy is known to over-estimate sleep [39].
Thus, it is highly likely that more individuals in this group
were simultaneously awake or in lighter, more easily aroused,
stages of sleep in a given epoch.
We calculated group sleep time as the duration from when
the first person was scored as asleep in the evening to when the
last person was scored as awake in the morning. Group sleep
was calculated to be 12 h, which is nearly double the average
individual sleep duration (table 1) and covers almost the
entire period of darkness experienced by this population.
Sleeping in a larger group will increase the number of
individuals who are awake, either through increased noise or
simply by chance. To assess whether the observed level of
simultaneously scored wakefulness differs from expectations
of randomly sleeping individuals, we used our Markov-
based null model with transitions between wake and sleep
states estimated from the empirical data, while variation
among individuals in sleep onset and offset times was ignored.
In other words, the null model represented individuals who
sleep independently of others and do not show variation in
chronotype. The observed mean number of individuals
scored as awake (8.65) was significantly higher than expected
from this model (mean of the distribution of the null
Table 1. Effective and individual sleep timing and duration. Specifically, 4
timing for effective group sleep is the period between when the first
rspb.royalsocietypublishing.org
person falls asleep and the last person wakes up. The individual average
for this group is measured as sleep onset and sleep end; note that the
additional time between onset and end is the individual averaged wake
after sleep onset (WASO) time of 2.4 h.
effective individual
parameter group sleep averaged sleep
sleep start 20.34 + 31 min 22.13 + 36 min
sleep end 07.48 + 20 min 06.55 + 28 min
Proc. R. Soc. B 284: 20170967
mean sleep duration 11.26 + 0.62 h 06.25 + 0.72 h
hypothesis ¼ 5.07, 95% of the simulated distribution was
from 4.15 to 5.95, with none of the 1000 simulated values
exceeding that which was observed). Additionally, we exam-
ined whether synchronous sleep is more extreme than
expected. We found that the observed value of 18 min of
scored synchronous sleep fell below the mean of the null distri-
bution (44.1), but within the 95% confidence interval from our
null model (11 to 117), and 10.9% of the distribution was more
extreme, i.e. smaller, than observed.
To further investigate patterns of activity, we ran FLM by
averaging the circadian actigraphy data for each individual
within the group. The output illustrated mean activity patterns
for individuals (figure 1), upon which we placed a horizontal
line representing a conservative estimate of sleep versus
wake determination. This line was placed at a threshold of 80
actigraphy counts per minute; thus, unlike the primary analy-
sis that used the high sensitivity threshold of 20 actigraphy
counts per minute to score sleep–wake epochs, we used a set-
ting that overestimates sleep scores and is thus (in this context)
a conservative estimate for inferring inactivity. In support of
the sentinel hypothesis, at no point in the 24 h period was
every individual inferred to be below this threshold.
(c) Potential sleep –wake pattern mechanisms
Several mechanisms could drive the unexpectedly high group-
level wakefulness that we documented. First, individuals could
show different chronotypes, with variation in sleep onset and
offset timing helping to ensure that more individuals are
awake throughout the night. Using circadian phase analysis,
we found that the Hadza CPM averaged as a group was
03:47 + 50, and that CPM varied significantly among individ-
uals (figure 2, ANOVA: F ¼ 14.11, d.f. ¼ 388, p , 0.001).
These findings are thus consistent with variation in chronotypes
among the subjects in our study, which reflects a mean chrono-
type based on night-to-night variation in sleep timing by each
individual. Second, the NREM-REM cycle is highly variable
in humans, as the average length of the first cycle is approxi-
mately 70–100 min, whereas later cycles shift to
approximately 90–120 min [40]. These cycles are associated
with brief episodes of arousal, usually involving REM sleep
transitions, and could thus influence general patterns of
sleep–wake transitions throughout the night. A third mechan-
ism could involve active asynchrony of sleep times throughout
the night. This might be achieved, for example, if individuals
prefer to sleep when others are awake, perhaps triggered via
background noise facilitating sleep by instilling a sense of
safety because others are awake. Alternatively, a single
 2500
2000
activity
1500
1000
500
0
midnight 6 AM
Figure 1. Functional linear modelling (FLM) analysis. Individual 24 h averaged activity (counts per minute) generated from FLM is compared among all individual
Hadza subjects throughout the 24 h period. The horizontal red line crosses the y-axis at ‘activity 80.’ This analysis reveals that several individuals exhibited moderate
levels of activity throughout the 24 h period in this population, and at no point did the averaged activity of all individuals fit under the conservative threshold of
80 activity counts per minute. In other words, more than one individual was inferred to be active throughout the 24 h period based on this analysis.
06.00
04.00
02.00
0
circadian phase measure of Hadza individuals
Figure 2. Circadian phase measure (CPM) in Hadza hunter – gatherers. CPM
is the midpoint clock time between sleep onset and awakening. Here, the
average CPM is illustrated for each individual with a beanplot, where the
horizontal white lines show the individual night-time CPM observations
and the black shows the distribution of the observed data; shape of the bean-
plot represents density. ANOVA revealed that the Hadza significantly differ in
CPM on the individual level (see §3c). Additionally, the more intra-individual
variation, the greater the spread from the red line; that is, the longer and
thinner the bean plots, the more variation is seen on the intra-individual
level. Note that the tails of the CPM distributions overlap several night-
time hours; in other words, variability in sleep timing is distributed through-
out the night-time period.
individual’s activity could promote multiple arousals as a type
of cascade effect, which could sustain a pool of awake individ-
uals, even if those awake tend to return to sleep.
We again used our simulation model of independently
sleeping individuals to investigate these possibilities, but this
time including chronotype variation across individuals by
simulating individual variation in inferred sleep onset and
offset based on the nightly data. We expected that observed
group wakefulness measures would fall outside of the simu-
lated distributions if active asynchrony is needed to achieve
the observed level of wakefulness, and within the simulated
distribution if chronotype variation is sufficient to achieve
the group wakefulness we observed. We found support for
the effect of chronotype variation on maintaining sentinel-
like behaviour: the observed mean of 8.65 individuals scored
as awake was well within the distribution of simulated
values from the model that included chronotype (mean ¼
8.94, 95% of distribution was from 7.73 to 10.2, and 32.3% of
simulated values were below 8.65). Similarly, the number
5
rspb.royalsocietypublishing.org
noon 6 PM midnight
time
Proc. R. Soc. B 284: 20170967
400
standardized central phase
300
measure
200
100
20 30 40 50 60
age
Figure 3. Plotted slope for the fixed coefficient of ‘age.’ Circadian phase
measure (CPM) was regressed on age, with circadian phase generated by cal-
culating each individual’s nightly number of minutes asleep from after
midnight. The model showed that sex, number of co-sleeping children, nur-
sing status and the study day (correcting for weather) did not significantly
influence CPM, but age did.
of epochs in which no individuals were scored as awake
(n ¼ 18) fell more clearly within the simulated distribution
(mean ¼ 12.4, 95% of distribution was from 0 to 38, with the
observed value marking the 90th percentile).
These results further raise the question of how chronotype
variation is maintained, which we tested cross-sectionally
in a linear mixed effects model. We found that variation in
chronotype (CPM) covaries with age, but not with other
fixed effects that include sex, co-sleeping, nursing status
and study day. That is, at older ages, individuals tend to exhi-
bit a more ‘lark’ type chronotype (age: b + s.e. ¼ 20.23 +
0.09, p ¼ 0.01, CI ¼ 20.401, 20.056; figure 3). Thus, variation
in age helps to generate variation in chronotype, which then
facilitates sentinel-like behaviour.
We also used the model to investigate the effects of group
size, aiming to assess the relative effects of group size and
chronotype variation on night-time safety in a more general
modelling framework that is not strictly tied to this population
and sampling regime. The model predicted that the mean
number of individuals awake scales linearly with group size
(figure 4a), and that the proportion of the time all individuals
are asleep drops asymptotically to zero with increasing
group size (figure 4b). Without variation in chronotypes, the
model revealed that group size would have to be substantially
larger to reach a similar level of safety as found with variation
in chronotype (figure 4).
 (a)
20
mean number awake
15
10
5 it has been defined as the distribution of bouts of wakefulness
0 chance [42]. In meerkats, for example, sentinel behaviour
10 20 30 40
(b)
6000
no. epochs all asleep
4000
2000
0 probabilities for arousal when such stimuli occur at these
10 20 30 40
group size
Figure 4. Simulating wakefulness dynamics in relation to group size. The
model used to assess significance of our results was also used to generally
examine predicted mean number of individuals awake (a) and number of
epochs in which all individuals were asleep (b), relative to group size.
Open circles indicate simulations with no variation in chronotype, while
filled circles incorporate variation in chronotype. Thus, variation in chronotype
increases substantially the mean number of individuals awake and, for groups
of 12 or fewer, reduces the duration of time when all individuals are asleep.
4. Discussion
These findings provide, to our knowledge, the first test of the
sentinel hypothesis in humans. We found that inter-individual
variation in chronotype and periodic awakenings are sufficient
to generate consistent sentinel-like behaviour throughout the
night for Hadza hunter–gatherers, without the need for any
active behavioural mechanisms, such as posting of actual senti-
nels, to maintain asynchrony. Furthermore, our model showed
that chronotype is not predicted by sex, environment, nursing
status or the number of co-sleeping children, but is a function
of age. Thus, on the basis of this research, we introduce the
poorly sleeping grandparent hypothesis for sentinel-like behav-
iour. That is, ancestral band level groups that exhibit variability
in age distribution would have facilitated adaptive sentinel-like
behaviour through greater variation in chronotypes.
That vigilance decreases as group size increases is one of the
most frequently reported relationships in the field of animal be-
haviour [41]. Our model may therefore explain why the Hadza
do not post sentinels at strategic locations throughout the night,
as typical sleeping group sizes may be sufficient to generate
sentinel-like behaviour. Interestingly, when group size drops
below a specific threshold much smaller than the groups we
studied, active sentinel behaviour is adopted. For example,
reports from San hunter–gatherers indicate that groups of
two to three males on long, multi-day hunting trips (to large
gatherings of animals at water holes) ensure that at least one
hunter is awake at all times (G. Yetish 2017, personal communi-
cation). As acknowledged above, our scoring based on
actigraphy does not necessarily mean that individuals scored 6
as ‘awake’ are truly awake and vigilant, as compared to studies
rspb.royalsocietypublishing.org
in other mammals where more direct observations of sentinel
behaviours are possible. Sentinel behaviour has often been
inferred by observation and anecdotal evidence, but rarely
has coordinated vigilance been systematically measured in
animal species; thus, in attempts to quantify sentinel behaviour,
across time that are more evenly distributed than expected by
has been measured as the proportion of time individuals are
bipedal with heads raised [42].
Proc. R. Soc. B 284: 20170967
A combination of observations, experiments, polysom-
nography and surveys would help to assess the degree
to which these inferred awakenings in the Hadza actually con-
tribute to sentinel behaviour, and the awareness by individuals
that they contribute to actual vigilance against threats. Even for
epochs representing light sleep or brief arousals (e.g. between
REM and NREM sleep stages), we propose that scored periods
of wakefulness would facilitate detection of threats from
conspecifics, predators and environmental risks, with higher
times. Future research could focus more directly on the role
that sleep architecture has in maintaining night-time vigilance
behaviour in humans.
Another relevant characteristic of sleep may be that sleep
phase is highly adaptable (i.e. flexible) in response to different
ecological, social and other factors, in humans [27,29] and
other animals [43]. The variation we documented in activity
patterns and chronotype (figures 1 and 2) reveals additional
evidence of flexibility characterizing sleep in the Hadza.
Flexibility may be characteristic of all human populations
today, representing a legacy of past selective pressures in fora-
ging populations. For example, the ‘first-night’ effect has been
observed to alter sleep in modern humans when sleeping in a
new environment, such as a hotel room, by shifting to a greater
reliance on sleep in one brain hemisphere and increasing
the other hemisphere’s sensitivity to deviant stimuli [44]. This
effect is similar to what is observed in birds and marine mam-
mals that sleep unihemispherically [45,46]. Use of EEG, coupled
with experimental increases or decreased in perceived threat,
could be used to test this idea in traditional populations,
although subject to ethical considerations for both EEG and
experimental manipulations.
Our research raises several new questions. For example,
could there be an optimal group size and mix of ages to achieve
more effective sentinel-like behaviour in human populations?
Sleep timing, duration, and staging changes throughout the
lifespan [47] and both chronotype [14] and sleep architecture
[48] are heritable. Therefore, an interesting question for future
work is to target the role that genes and environment play
in the timing and duration of sleep throughout different life-
history stages. Another direction for future research concerns
ways that natural selection could promote individual variabil-
ity in chronotype, which would be in addition to the variation
we demonstrated in relation to age. Genetic variation in chron-
otype could be maintained by frequency-dependent selection,
such that individuals with rare chronotypes in a population are
favoured [49]. Such selection might occur if advantages accrue
at the individual level to being awake when most others are
asleep. For example, quiet times represent opportunities for
attacks by predators or conspecifics, and being awake while
others sleep would conceivably reduce individual mortality
risk in such conditions. Additionally, group and/or kin selec- immunity to predators. . .either by their own defensive strength 7
tion could favour groups of individuals that show more or. . .inaccessibility for protection during sleep.’ This prediction

chronotype variation [50,51]. Variability in chronotype could
be further enhanced through sexual selection, perhaps as indi-
cated by variation in reproductive success among chronotypes
in Western populations [52]. Alternatively, greater flexibility in
sleep patterns could emerge simply from relaxed selection on a
specific chronotype in our evolutionary past.
Our findings also have implications for evolutionary per-
spectives on sleep disorders. Disorders of circadian rhythm
are defined by a mismatch between the desired sleep demands
of the social environment and that of an individual’s natural
rspb.royalsocietypublishing.org
has since been supported in phylogenetic analyses showing
that mammalian species that experience a greater risk of preda-
tion at the sleep site exhibited less REM sleep [56,57] and that
humans have both shorter than expected sleep and a higher
than expected proportion of REM sleep [58]. Throughout
human evolution, the transition to relatively deeper, higher
quality sleep would have conferred cognitive benefits such as
the consolidation of memory [59], processing of emotion lead-
ing to better social intelligence [60], and increasing creativity
and innovation [61]. The success of Homo sapiens has been

Proc. R. Soc. B 284: 20170967

sleep period [18,53]. Specifically, circadian rhythm disorders
are characterized by three types of sleep timing mismatch:
(i) advanced sleep phase syndrome, in which affected individuals
tend to fall asleep earlier and wake up earlier than preferred,
(ii) delayed sleep phase syndrome, in which affected individuals
tend to go to bed later and sleep later than is preferred, and
(iii) irregular sleep–wake schedule, where a shifting mismatch
occurs between the period in which an individual is able
to sleep and their preferred sleep period. The mechanisms
generating variation in sleep durations and patterning may
have resulted in disorders of circadian rhythms in modern
populations, especially when coupled with lifestyle and tech-
nological changes, such as access to artificial lighting, that
may accentuate variation in chronotypes [54]. Our results
also shed new light on clinical reports of ‘insomnia’ among
older individuals. For example, modern perspectives often
hold that changes in sleep duration and timing in the elderly
are a disorder to treat [55]; by normalizing ‘wakeful grand-
parents,’ thereby downplaying the ‘sick role’ among older
individuals, clinicians could promote health by reducing
overmedication among older individuals.
Intriguingly, Snyder [1] initially postulated (p. 132), ‘. . ..that
sleep would have the greatest continuity and the REM state
would be best developed in those forms with the highest
described as ‘a spectacular evolutionary anomaly’ that has
resulted in humans colonizing every terrestrial habitat [62].
Sleep, facilitated by sentinel-like behaviour, was one part
of the adaptive suite of characters that led to humanity’s
evolutionary success.
Ethics. All research was approved by the Tanzanian Commission for
Science and Technology (COSTECH), the Tanzanian National Insti-
tute for Medical Research (NIMR) and the Institutional Review
Board for human subjects research at the University of Nevada, Las
Vegas and Duke University.
Data accessibility. The raw data will be archived in DRYAD data
repository.
Authors’ contributions. D.R.S., A.N.C. and C.L.N. designed research;
D.R.S., I.A.M. and A.Z.P.M. performed research; D.R.S. analysed
data; D.R.S., A.N.C. and C.L.N. wrote the paper.
Competing interests. We declare we have no competing interests.
Funding. This grant was funded by National Geographic (grant no.
9665-15).
Acknowledgements. We would like to thank the Hadza, the Tanzanian
Commission for Science and Technology (COSTECH) and the
Tanzanian National Institute for Medical Research (NIMR)
for research approval. We appreciate insightful feedback on the
manuscript from Andrew Phillips, James McKenna, Gandhi
Yetish and anonymous reviewers.

References
1. Snyder F. 1966 Toward an evolutionary theory of
dreaming. Am. J. Psychiatry 123, 121 –136. (doi:10.
1176/ajp.123.2.121)
2. Beauchamp G. 2015 Animal vigilance: monitoring
predators and competitors. Quebec, Canada:
Academic Press.
3. Randler C. 2014 Sleep, sleep timing and chronotype
in animal behaviour. Anim. Behav. 94, 161–166.
(doi:10.1016/j.anbehav.2014.05.001)
4. Von Aschoff J, Wever R. 1962 Spontanperiodik des
menschen bei ausschluss aller zeitgeber.
Naturwissenschaften 49, 337 –342. (doi:10.1007/
BF01185109)
5. Steinmeyer C, Schielzeth H, Mueller JC,
Kempenaers B. 2010 Variation in sleep behaviour
in free-living blue tits, Cyanistes caeruleus: effects of
sex, age and environment. Anim. Behav. 80, 853–
864. (doi:10.1016/j.anbehav.2010.08.005)
6. Wicht H, Korf HW, Ackermann H, Ekhart D, Fischer
C, Pfeffer M. 2014 Chronotypes and rhythm stability
in mice. Chronobiol. Int. 31, 27 –36. (doi:10.3109/
07420528.2013.820739)
7. Labyak SE, Lee TM, Goel N. 1997 Rhythm
chronotypes in a diurnal rodent, Octodon degus.
Am. J. Physiol 273, R1058– R1066.
8. Roenneberg T, Kuehnle T, Pramstaller PP, Ricken J,
Havel M, Guth A, Merrow M. 2004 A marker for the
end of adolescence. Curr. Biol. 14, R1038–R1039.
(doi:10.1016/j.cub.2004.11.039)
9. Baehr EK, Revelle W, Eastman CI. 2000 Individual
differences in the phase and amplitude of the
human circadian temperature rhythm: with an
emphasis on morningness–eveningness. J. Sleep
Res. 9, 117–127. (doi:10.1046/j.1365-2869.2000.
00196.x)
10. Sarabia J, Rol M, Mendiola P, Madrid J. 2008
Circadian rhythm of wrist temperature in normal-
living subjects: a candidate of new index of the
circadian system. Physiol. Behav. 95, 570 –580.
(doi:10.1016/j.physbeh.2008.08.005)
11. Burgess HJ, Fogg LF. 2008 Individual differences in
the amount and timing of salivary melatonin
secretion. PLoS ONE 3, e3055. (doi:10.1371/journal.
pone.0003055)
12. Randler C, Schaal S. 2010 Morningness –
eveningness, habitual sleep–wake variables and
cortisol level. Biol. Psychol. 85, 14 –18. (doi:10.
1016/j.biopsycho.2010.04.006)
13. Randler C, Ebenhöh N, Fischer A, Höchel S, Schroff
C, Stoll JC, Vollmer C. 2012 Chronotype but not
sleep length is related to salivary testosterone in
young adult men. Psychoneuroendocrinology 37,
1740– 1744. (doi:10.1016/j.psyneuen.2012.02.008)
14. Lopez-Minguez J, Ordoñana JR, Sánchez-Romera JF,
Madrid JA, Garaulet M. 2015 Circadian system
heritability as assessed by wrist temperature: a twin
study. Chronobiol. Int. 32, 71 –80. (doi:10.3109/
07420528.2014.955186)
15. Viola AU, Archer SN, James LM, Groeger JA, Lo JCY,
Skene DJ, von Schantz M, Dijk DJ. 2007 PER3
polymorphism predicts sleep structure and waking
performance. Curr. Biol. 17, 613 –618. (doi:10.
1016/j.cub.2007.01.073)
16. Patke A, Murphy PJ, Onat OE, Krieger AC, Özçelik T,
Campbell SS, Young MW. 2017 Mutation of the
human circadian clock gene CRY1 in familial delayed
 sleep phase disorder. Cell 169, 203– 215. (doi:10.
1016/j.cell.2017.03.027)
17. Reid KJ, Zee PC. 2011 Circadian disorders of the
sleep– wake cycle. In Principles and practice of
sleep medicine (eds MH Kryger, T Roth, WC
Dement), pp. 470 –482. St. Louis, MO: Elsevier
Saunders.
18. Nunn CL, Samson DR, Krystal A. 2016 Shining
evolutionary light on human sleep and sleep
disorders. Evol. Med. Public Health 1, 227– 243.
(doi:10.1093/emph/eow018)
19. Marlowe FW. 2010 The Hadza: hunter –gatherers of
Tanzania. Berkeley, CA: University of California Press.
20. Marlowe FW. 2006 Central place provisioning, the
Hadza as an example. In Feeding ecology in apes
and other primates (eds G Hohmann, MM Robbins),
pp. 359– 379. Cambridge, UK: Cambridge University
Press.
21. Crittenden AN. 2016 Ethnobotany in evolutionary
perspective: wild plants in diet composition and
daily use among Hadza hunter –gatherers. In Wild
harvest: plants in the hominin and pre-agrarian
human worlds (eds K Hardy, ML Kubiak),
pp. 319 –339. Oxford, UK: Oxbow Books.
22. Crittenden AN. 2014 Ancestral attachment. In
Ancestral landscapes in human evolution: culture,
childrearing and social wellbeing (eds D Narvaez, K
Valentino, F Agustin, J McKenna, JP Gray), p. 282.
Oxford, UK: Oxford University Press.
23. Apicella CL, Crittenden AN. 2015 Hunter – gatherer
families and parenting. In The handbook of
evolutionary psychology (ed. DM Buss),
pp. 797 –827. Hoboken, NJ: Wiley Publishing.
24. Barry H, Paxson LM. 1971 Infancy and early
childhood: cross-cultural codes. Ethnology 10,
466–508. (doi:10.2307/3773177)
25. Kanady JC, Drummond S, Mednick SC. 2011
Actigraphic assessment of a polysomnographic-
recorded nap: a validation study. J. Sleep Res. 20,
214–222. (doi:10.1111/j.1365-2869.2010.00858.x)
26. Knutson KL. 2014 Sleep duration, quality, and
timing and their associations with age in a
community without electricity in Haiti. Am. J. Hum.
Biol. 26, 80 –86. (doi:10.1002/ajhb.22481)
27. Samson DR, Manus MB, Krystal AD, Fakir E, Yu JJ,
Nunn CL. 2017 Segmented sleep in a nonelectric,
small-scale agricultural society in Madagascar.
Am. J. Hum. Biol. (doi:10.1002/ajhb.22979)
28. Yetish G, Kaplan H, Gurven M, Wood B, Pontzer H,
Manger PR, Wilson C, McGregor R, Siegel JM. 2015
Natural sleep and its seasonal variations in three
pre-industrial societies. Curr. Biol. 25, 1–7. (doi:10.
1016/j.cub.2015.09.046)
29. Samson DR, Crittenden AN, Mabulla IA, Mabulla AZP,
Nunn CL. 2017 Hadza sleep biology: evidence for flexible
sleep–wake patterns in hunter–gatherers. Am. J. Phys.
Anthropol. 162, 399–610. (doi:10.1002/ajpa.23160)
30. Sri Kantha S, Suzuki J. 2006 Sleep quantitation in
common marmoset, cotton top tamarin and squirrel
monkey by non-invasive actigraphy. Comp. Biochem.
Physiol. A Mol. Integr. Physiol. 144, 203–210.
(doi:10.1016/j.cbpa.2006.02.043)
31. Ermis U, Krakow K, Voss U. 2010 Arousal thresholds
during human tonic and phasic REM sleep. J. Sleep Res.
19, 400–406. (doi:10.1111/j.1365-2869.2010.00831.x)
32. R Core Team. 2016 R: a language and environment
for statistical computing. Vienna, Austria.
33. Shannon W, Li T, Xian H, Wang J, Deych E, Gonzalez
C. 2015 Functional Actigraphy Data Analysis.
Package ‘Actigraphy’. See CRAN repository: https://
cran.r-project.org/web/packages.
34. Van Someren EJ, Swaab DF, Colenda CC, Cohen W,
McCall WV, Rosenquist PB. 1999 Bright light therapy:
improved sensitivity to its effects on rest–activity
rhythms in Alzheimer patients by application of
nonparametric methods. Chronobiol. Int. 16,
505–518. (doi:10.3109/07420529908998724)
35. Bates D, Maecher M, Bolker B, Walker, S. 2015
Fitting linear mixed-effects models using lme4.
J. Stat. Softw. 67, 1 –48. (doi:10.18637/jss.v067.i01)
36. Burnham K, Anderson D. 2002 Information and
likelihood theory: a basis for model selection and
inference. In Model selection and multimodel
inference: a practical information-theoretic approach,
2nd edition, pp. 49–97. New York, NY: Springer.
37. Bartoń K. 2015 Version 1.15.6 ed. See https://cran.r-
project.org/web/packages/MuMIn.
38. Samson DR, Crittenden AN, Mabulla AI, Mabulla I,
Nunn CL. In review. The evolution of a good night’s
rest: technological and cultural innovation
associated with sleep in Hadza hunter –gatherers.
J. Hum. Evol.
39. Stone KL, Ancoli-Israel A. 2011 Actigraphy. In
Principles and practice of sleep medicine (eds MH
Kryger, T Roth, C William), pp. 1668–1675.
St. Louis, MO: Elsevier Saunders.
40. Carskadon MA, Dement WC. 2005 Normal human
sleep: an overview. In Principles and practice in sleep
medicine, 4th edn (eds MH Kryger, T Roth, WC
Dement), pp. 13– 23. Philadelphia, PA: Elsevier
Saunders.
41. Roberts G. 1996 Why individual vigilance declines
as group size increases. Anim. Behav. 51,
1077 –1086. (doi:10.1006/anbe.1996.0109)
42. Bednekoff PA. 2015 Chapter Four—Sentinel
behavior: a review and prospectus. In Advances in
the study of behavior, vol. 47 (eds M Naguib, JBS
Peter), pp. 115 –145. Waltham, MA: Academic
Press.
43. Tobler I. 1989 Napping and polyphasic sleep in
mammals. In Sleep and alertness: chronobiological,
behavioral, and medical aspects of napping (eds DF
Dinges, RJ Broughton), pp. 9–30. New York, NY:
Raven Press, Ltd.
44. Tamaki M, Bang Ji W, Watanabe T, Sasaki Y. 2016 Night
watch in one brain hemisphere during sleep associated
with the first-night effect in humans. Curr. Biol. 26,
1190–1194. (doi:10.1016/j.cub.2016.02.063)
45. Rattenborg NC, Voirin B, Cruz SM, Tisdale R, Dell-
Omo G, Lipp HP, Wikelski M, Vyssotski AL. 2016
Evidence that birds sleep in mid-flight. Nat.
Commun. 7, 1–9. (doi:10.1038/ncomms12468)
46. Lyamin O, Manger P, Ridgway S, Mukhametov L,
Siegel J. 2008 Cetacean sleep: an unusual form of
mammalian sleep. Neurosci. Biobehav. Rev. 32, 8
1451– 1484. (doi:10.1016/j.neubiorev.2008.05.023)
rspb.royalsocietypublishing.org
47. Ohayon MM, Carskadon MA, Guilleminault C,
Vitiello M. 2004 Meta-analysis of quantitative sleep
parameters from childhood to old age in healthy
individuals: developing normative sleep values
across the human lifespan. Sleep 27, 1255–1273.
48. Kuna ST, Maislin G, Pack FM, Staley B, Hachadoorian R,
Coccaro EF, Pack AI. 2012 Heritability of performance
deficit accumulation during acute sleep deprivation in
twins. Sleep 35, 1223–1233. (doi:10.5665/sleep.2074)
49. Ayala FJ, Campbell CA. 1974 Frequency-dependent
Proc. R. Soc. B 284: 20170967
selection. Annu. Rev. Ecol. Syst. 5, 115– 138.
(doi:10.1146/annurev.es.05.110174.000555)
50. Nowak MA, Tarnita CE, Wilson EO. 2010 The
evolution of eusociality. Nature 466, 1057–1062.
(doi:10.1038/nature09205)
51. Marshall JAR. 2011 Group selection and kin
selection: formally equivalent approaches. Trends
Ecol. Evol. 26, 325–332. (doi:10.1016/j.tree.2011.
04.008)
52. Randler C, Ebenhöh N, Fischer A, Höchel S, Schroff
C, Stoll JC, Vollmer C, Piffer D. 2012 Eveningness is
related to men’s mating success. Pers. Individ. Dif.
53, 263 –267. (doi:10.1016/j.paid.2012.03.025)
53. Jones CR, Huang AL, Ptáček LJ, Fu YH. 2013 Genetic
basis of human circadian rhythm disorders. Exp.
Neurol. 243, 28 –33. (doi:10.1016/j.expneurol.2012.
07.012)
54. Pandi-Perumal S, Seils L, Kayumov L, Ralp M, Lowe
A, Moller H, Swaab D. 2002 Senescence, sleep, and
circadian rhythms. Ageing Res. Rev. 1, 559–604.
(doi:10.1016/S1568-1637(02)00014-4)
55. Wright KP, McHill AW, Birks BR., Griffin BR,
Rusterholz T, Chinoy ED. 2013 Entrainment of the
human circadian clock to the natural light –dark
cycle. Curr. Biol. 23, 1554–1558. (doi:10.1016/j.
cub.2013.06.039)
56. Capellini I, Barton RA, McNamara P, Preston B,
Nunn CL. 2008 Ecology and evolution of
mammalian sleep. Evolution 62, 1764–1776.
(doi:10.1111/j.1558-5646.2008.00392.x)
57. Lesku JA, Roth TC, Amlaner CJ, Lima SL. 2006 A
phylogenetic analysis of sleep architecture in mammals:
the integration of anatomy, physiology, and ecology.
Am. Nat. 168, 441–453. (doi:10.1086/506973)
58. Samson DR, Nunn CL. 2015 Sleep intensity and the
evolution of human cognition. Evol. Anthropol. 24,
225–237. (doi:10.1002/evan.21464)
59. Walker MP, Stickgold R. 2004 Sleep-dependent
learning and memory consolidation. Neuron 44,
121–133. (doi:10.1016/j.neuron.2004.08.031)
60. Walker MP. 2009 The role of sleep in cognition and
emotion. Ann. N. Y. Acad. Sci. 1156, 168 –197.
(doi:10.1111/j.1749-6632.2009.04416.x)
61. Wagner U, Gais S, Haider H, Verleger R, Born J.
2004 Sleep inspires insight. Nature 427, 352 –355.
(doi:10.1038/nature02223)
62. Hill K, Barton M, Hurtado AM. 2009 The emergence
of human uniqueness: characters underlying
behavioral modernity. Evol. Anthropol. 18,
187–200. (doi:10.1002/evan.20224)